Plankton Benthos Res 7(4): 188–194, 2012 Plankton & Benthos Research © The Plankton Society of Japan

Seasonal succession of four (Copepoda, ) in Okkirai Bay, Sanriku, northern Japan

YUICHIRO YAMADA*, ATSUSHI KOBIYAMA & TAKEHIKO OGATA

School of Marine Biosciences, Kitasato University, 1–15–1 Kitasato, Minami-ku, Sagamihara 252–0329, Japan Received 17 April 2012; Accepted 4 September 2012

Abstract: Seasonal changes in abundance of four neritic Acartia species (A. hudsonica, A. omorii, A. longiremis and A. steueri), including identifiable copepodid stages, were investigated in the inner reaches of Okkirai Bay, Sanriku, northern Japan, to elucidate their seasonal succession patterns. Samples were collected monthly at intervals from Au- gust 2007 to July 2009 by vertical hauls of a NORPAC net of 100 μm mesh aperture. For identification of morphologi- cally allied A. omorii and A. hudsonica, the dimensional differences between them were statistically analyzed for the stages of C4 to C6. The dominant species were A. longiremis in the colder season and A. steueri in the warmer sea- son. A. longiremis and A. omorii appeared from early spring (February or March) to summer with numerical peaks in April. These April peaks were considered to result from immigration from outside the bay with intrusions of Oyashio Current water. A. steueri increased during the summer with a peak in September, then decreased until December or January, and disappeared for two or three months from April, when they were probably only present as diapausing eggs. A. hudsonica occurred from early spring to mid-summer as in A. omorii but with higher abundances in summer than in spring, though the seasonal abundances varied somewhat between years. These results suggest that tempera- ture, determining reproductive activity (and production of diapausing eggs in A. steueri), and intrusions of Oyashio water are important environmental factors determining seasonal succession of acartiid copepods in the bay.

Key words: Acartia, copepods, Oyashio water, Sanriku, seasonal succession

1976, A. longiremis (Lilljeborg, 1853) and A. steueri Introduction Smirnov, 1936 commonly inhabit in the inlet waters Acartia spp. are typical calanoid copepods that occur in (Terazaki 1980, Uye 1982, Ueda 1986b, Saito & Taguchi coastal and inlet waters across the world from boreal to 1996, Seki & Shimizu 1997). However, information on tropical regions (Bradford 1976, Mauchline 1998). They their seasonal succession is still not enough in northern are major copepods in these waters and their numbers Japan. In the present study, we investigated the seasonal sometimes reach more than 20,000 ind. m－3 (e.g. Onoue et changes in abundances of acartiid copepods, including im- al. 2006). They are important not only as consumers of mature copepodids, for two years in Okkirai Bay, a small phytoplankton and microzooplankton (Putland & Iverson inlet on the Rias coast of the Sanriku area, northern Japan, 2007) but also as prey for fish larvae (Seki & Shimizu and discussed the relationship between their seasonal oc- 1997). Thus, acartiid copepods are key organisms to link currence and the environmental factors. the primary producers and the secondary consumers in coastal and inlet waters (Putland & Iverson 2007). In tem- Materials and Methods perate waters of Japan, seasonal changes in the geographi- cal distribution and community structure of Acartia spe- Field sampling cies are well documented (Ueda 1987, Uye et al. 2000). In the coastal areas of Tohoku and Hokkaido in northern Field sampling was carried out almost every month for Japan, A. hudsonica Pinhey, 1926, A. omorii Bradford, two years from August 2007 to July 2009 at an inner sta- tion of Okkirai Bay, which faces the northwestern Pacific * Corresponding author: Yuichiro Yamada; E-mail, yyamada@kitasato- Ocean (Fig. 1). The water depth at the sampling site ranged u.ac.jp Seasonal succession of four Acartia species 189

Table 1. List of sampling date, volume of the water filtered, and aliquot of sample examined.

Volume of Aliquot Year Date the water filtered examined (m3)

2007 30 Aug 0.82 1/1 19 Sep 2.49 1/4 17 Oct 2.03 1/4 16 Nov 2.10 1/1 20 Dec 2.42 1/1 2008 15 Jan 2.10 1/1 Fig. 1. Sampling site in Okkirai Bay, Sanriku, northern Japan. 19 Feb 2.03 1/1 25 Mar 2.23 1/1 17 Apr 1.37 1/2 from 17 to 19 m depending on the tide. Zooplankton sam- 15 May 1.82 1/1 ples were collected by vertical hauls of a NORPAC net 20 Jun 1.16 1/2 (mouth opening 45 cm, mesh size 100 μm) from the near- 22 Jul 1.44 1/1 bottom to the surface, and were preserved in 5% buffered 18 Aug 4.44 1/2 formalin seawater immediately after sampling. The 16 Sep 2.30 1/4 amount of water filtered was measured with a flow meter 17 Oct 2.51 1/1 (5571-A, Rigosha Co., Ltd., Japan) set at the mouth of the 18 Nov 2.61 1/2 net; the filtered volumes are presented in Table 1. Vertical 15 Dec 2.30 1/1 2009 28 Jan 1.84 1/1 profiles of temperature, salinity, and chlorophyll a concen- 12 Feb 2.09 1/2 tration were determined for each 0.1 m using a CTD sys- 13 Mar 2.34 1/1 tem equipped with a chlorophyll fluorescence sensor 17 Apr 0.81 1/4 (ACL200-PDK, JFE Alec Co., Ltd., Japan). 23 May 1.87 1/1 13 Jun 0.96 1/1 Developmental stage analysis and species identification 16 Jul 1.85 1/1 All copepodids and adults of Acartia spp. were sorted, under a dissecting microscope from the entire samples, or 1/2 or 1/4 aliquots (Table 1) when too many acartiid cope- 1986b). However, these diagnostic characters cannot be pods were collected. The sorted copepods were then sepa- used for identification of immature copepods and are rated into nine groups according to the ontogenetic stages sometimes difficult to observe without dissection, even in (C1–C6) and sexes (female and male of C4–C6) following adult copepods. Accordingly we classified them into the Sabatini (1990). Since no morphological characteristics en- two species by prosome length, which is known to be abling the species to be differentiated could be found in larger in A. omorii than in A. hudsonica (Ueda 1986b). To C1, they were not classified into species. In C2 and higher test the criteria of length for separating the species, all of stages, A. steueri could be distinguished from other acar- these C4–C6 individuals were photographed using a digi- tiid copepods by the presence of rostral filaments, which tal camera equipped on a microscope, and their prosome were absent in the other three species. As for the other lengths were measured to the nearest 0.01 mm using three species, no species-specific morphologies enabling ImageJ® software (NIH, USA). The results showed that the us to distinguish the species from each other were ob- prosome length distribution was apparently bimodal in served in either C2 or C3, and they were counted without every stage and sex (Fig. 2) with boundaries at 0.85 mm species discrimination. Acartia longiremis could be identi- for C6 females and 0.79 mm for C6 males. Three hundred fied by having spinules along the posterodorsal margins of and twenty seven individuals of C6 females (150 for the the urosomites in C4 and higher stages. larger mode and 177 for the smaller mode) and 129 individ- Since acartiid copepods identifiable to species other uals of C6 males (76 for the larger mode and 53 for the than the present four species did not occur in our samples, smaller mode) were examined for the diagnostic characters C4 and higher stages without rostral filaments and/or uro- used in the identification of each species. The individual somal spinules could be identified as either A. omorii or A. numbers of A. omorii and A. hudsonica were 145 and 5 for hudsonica. The two species can be distinguished by the the larger mode, and 8 and 169 for the smaller mode in C6 length/width ratio of the genital double somite of adult fe- females. For C6 males, larger and small modes were deter- males (<1.1 for A. omorii and ≥1.1 for A. hudsonica) and by mined as A. omorii and A. hudsonca without exception. To the number of convex surfaces in the inner lobe of the determine the boundary between the species in both sexes, third segment of the fifth right leg of adult males (2 for A. a linear discriminant (Goebel et al. 2007) calculated with omorii and 1 for A. hudsonica) (Bradford 1976, Ueda the Mulcel® software program (OMS Publishing Inc.) re- 190 Y. Yamada et al.

Fig. 2. Prosome length distribution of all C4–C6 (adult) copepods of Acartia omorii and A. hudsonica collected from Okki- rai Bay from April 2007 to July 2009. Arrows indicate the boundary lengths calculated by the linear discriminant function analysis. vealed that A. omorii and A. hudsonica could be classified with 96.7 and 99.4% probability, respectively, with a boundary at 0.85 mm for C6 females, and both at 100% probability at 0.79 mm for C6 males. Although the size dis- tributions of the two species overlapped each other in some cases, the number of individuals beyond the boundary be- tween the modes was considered negligible compared with the total number individuals in each mode.

Results

Water temperature increased from March to September Fig. 3. Seasonal changes in temperature, salinity, and chloro- with the minimum temperature of 4.4°C in March 2008 phyll a concentration in Okkirai Bay. The values are vertical and the maximum of 20.3°C in September 2007 (Fig. 3). means from 0 to 17 m depth. The annual minimum temperature was recorded in March in both 2008 and 2009, but was much lower in 2008 (4.4°C) than in 2009 (6.2°C). Salinity varied between 33.2 species are shown in Fig. 4, in which the species-specific in March and April 2008 to 34.2 in December 2007. High data are presented by compiling the stages for which the salinities (>33.7) were observed from October 2007 to Feb- species were distinguished, i.e. C2–C6 for A. steueri and ruary 2008 and from October 2008 to March 2009, and C4–C6 for the other three species. Seasonal abundances of low salinities (<33.5) occurred from March 2008 to May unidentified C1 and C2–C3 of the species other than A. 2008 and in September 2008 and June 2009. Chlorophyll a steueri are also presented. concentration exhibited annual peaks in March 2008 Acartia steueri C2–C6 was abundant (>200 ind. m－3) (2.13 μg L－1) and April 2009 (1.81 μg L－1). In 2008, the from August to November 2007 and from September to concentration decreased to the season’s lowest (0.63 μg L－1) October 2008 with prominent annual peaks in September in January 2009, partially recovering in June and October. 2007 and 2008 (6,055 and 1,491 ind. m－3, respectively), Seasonal variations in the abundance of the four Acartia while it was less abundant (<100 ind. m－3) from December Seasonal succession of four Acartia species 191 to June or July and was not detected from April to June Discussion 2008 or from April to May 2009 (Fig. 4a). Since the first month (August 2007) of this study, this species was ex- The present study showed clear seasonal succession of tremely abundant (>1,000 ind. m－3) until October 2007 and Acartia species in Okkirai Bay. Acartia longiremis and A. was the only species in the Acartia community for six omorii were abundant during the three to six colder months until A. omorii appeared in February 2008. months from February or March with the highest annual Acartia longiremis C4–C6 was absent from August abundance in February to April. In contrast, A. steueri was 2007 to February 2008, but suddenly appeared in March more abundant during warmer months than in colder 2008 with a relatively high abundance (204 ind. m－3) and months, and exhibited extremely high abundances from soon reached the peak abundance (1,317 ind. m－3) in April August to October. The abundance of A. hudsonica was (Fig. 4b). Then it greatly decreased in number to also higher during warmer months than in colder months. 12 ind. m－3 in June, and completely disappeared from Au- Occurrences of A. longiremis have been reported from gust 2008 to January 2009 with the exception of a low cold waters in the northern Pacific and northern Atlantic abundance (16 ind. m－3) in September 2008. In 2009, the Oceans and at their margins, e.g. western Greenland species began its seasonal occurrence in February and ex- (Madsen et al. 2008), the Chukchi Sea (Hopcroft et al. hibited a peak (2,602 ind. m－3) in April after it decreased 2010), Faroe Islands (Debes et al. 2008), southwestern once in March. The peaks in both years were coincident Alaska (Park et al. 2004), an estuary in Maine, USA (Lee with the annual maxima of chlorophyll a concentrations & McAlice 1979), and the Oregon coast (Keister & Peter- and were one month later than the annual lowest tempera- son 2003). Lee & McAlice (1979) reported that A. longire- tures. mis disappeared in August, when water temperature The seasonal pattern of A. omorii C4–C6 was similar to reached the annual maximum (>15°C), and reappeared that of A. longiremis with high abundances during the soon in September. In Okkirai Bay, the C4–C6 stages of A. springs and low abundances during the summers and falls longiremis began their seasonal occurrence by a sudden in- (Fig. 4c). However, the annual peak abundances of both crease in February or March with subsequent prominent years (283 ind. m－3 in April 2008 and 229 ind. m－3 in Feb- peaks in April, and disappeared from the mid or late sum- ruary 2009) were much less than those of A. longiremis, mer until the following spring. If they were reproducing and the period when the species was completely absent in within the bay, abundance peaks of the unidentifiable C2– 2008 was shorter (two months from October to November) C3 copepodids should have appeared before the first in- than in A. longiremis (four months from October to Janu- crease of the C4–C6 stages. However, the present study ary). did not show such a peak for C2–C3 in 2008, that is, the Acartia hudsonica C4–C6 occurred from March to Sep- C4–C6 stages began to increase in March, whereas the tember 2008 and from February 2009 to the end of the C2–C3 stages were completely or almost absent until study period in July 2009 with the occurrence of a small March. In 2009, the C2–C3 population exhibited a similar number in December 2008 (Fig. 4d). This seasonal occur- change from January to April to that of C4–C6 but a small rence pattern was similar to those of A. longiremis and A. increase in December 2008, two months before the first in- omorii, but the annual maximum abundances (104 ind. m－3 crease of C4–C6. The C2–C3 population in December in September 2008 and 140 ind. m－3 in June 2009) were 2008 is highly unlikely to have grown into C4–C6 by Feb- not in sharp peaks and occurred during the warmer months ruary 2009, because two months is too long a period for (September 2008 and June 2009) in contrast to the colder development from C2–C3 to C4–C6. Considering that the months in A. longiremis and A. omorii. The abundances 2008 population of A. longiremis C4–C6 suddenly ap- during mid-summer (August and September) differed peared at high abundances in March without a preceding greatly between 2007 and 2008; the species was absent in peak in abundances for the younger stages, it is likely that 2007 while it reached its annual maximum in 2008. they were not reproducing in the bay but were introduced Unidentified C1 copepods showed prominent peaks through lateral advection from outside the bay. The most twice a year, i.e. one in spring (April) and the other in late plausible explanation for the immigration is with intrusion summer (September 2007 and October 2008) (Fig. 4e). Un- of Oyashio Current water. Takasugi & Yasuda (1994) dem- identified C2 and C3 consisting of A. longiremis, A. omo- onstrated that Oyashio Current water appeared along the rii, and/or A. hudsonica exhibited clear seasonality with Sanriku coast most frequently from March to April and sudden peaks in April in both 2008 and 2009 (780 and least from November to December. These months coincide 1,072 ind. m－3, respectively) and a secondary peak in June precisely with those of the annual highest abundances and 2008 (280 ind. m－3). They were completely or nearly ab- absence of A. longiremis C4–C6 in Okkirai Bay, respec- sent from August 2007 to March 2008, and exhibited a tively. Despite the location of the sampling station in the small increase in December 2008. This seasonal pattern of innermost part of the bay, where the land runoff and air C2–C3 was most similar to that of A. longiremis. temperature generally have strong effects on in situ condi- tions, the low temperature (4.4°C) and low salinity (33.2) observed at the station in March 2008, when A. longiremis 192 Y. Yamada et al.

Fig. 4. Seasonal changes in abundance of Acartia steueri (a), A. longiremis (b), A. omorii (c), and A. hudsonica (d), with those of unidentified C1 (e) and C2–C3 (f), in Okkirai Bay.

C4–C6 suddenly increased, were very similar to those of pears when the water temperature rises above 15°C (Ya- surface waters of the Oyashio Current reported in the same mada, unpublished data). Because the highest tolerable month (Japan Oceanographic Data Center 2008). These ob- temperature for Pseudocalanus spp. has been estimated to servations suggest that in March and April Oyashio Cur- be 12–15°C (Yamaguchi & Shiga 1997), these copepods rent water had extensively intruded into the bay, bringing probably cannot reproduce in Okkirai Bay when the water with it the A. longiremis population. Lee & McAlice (1979) temperature rises beyond 15°C in July (see Fig. 3). In con- also suggested that immigration from coastal waters was trast to Pseudocalanus spp., A. longiremis occurred even necessary for the maintenance of the A. longiremis popula- in September 2008 when the water temperature was tion in an estuary in Maine. 19.9°C, indicating that this is tolerable of higher In Okkirai Bay, the cold-water copepod Pseudocalanus temperatures than Pseudocalanus spp. although it cannot spp. appears with intrusions of Oyashio water, and disap- reproduce for year-round maintenance of populations in Seasonal succession of four Acartia species 193 the bay. strongly enclosed bays to open oceanic waters such as The abundance of A. steueri C2–C6 peaked in Septem- 300 km off the Pacific coast of Honshu, and was the exclu- ber when the water temperature reached its maximum sively dominant copepod in samples collected from oce- (around 20°C), and was low from December or January to anic waters off Hokkaido and Honshu. Such distributional June or July. Kang & Kang (2005) and Onoue et al. (2006) characteristics of A. omorii suggest that immigration from reported that A. steueri was most abundant at around 20°C outside Okkirai Bay with intrusion of Oyashio Current from July to August in Ilkwang Bay on the southeastern water may have resulted in its high abundance in April, as coast of Korea and from May to June in Sagami Bay, cen- suggested for the changes in seasonal abundance of A. lon- tral Japan, respectively. This suggests that 20°C is the opti- giremis. As for the “eutrophic neritic” copepod A. hudson- mum temperature for their growth and reproduction. The ica, recruitment from outside the bay is unlikely. Instead, abundances of A. steueri in these bays were very low when the seasonal abundance of this species at the sampling site the water temperatures reached the maxima (26.8 and is considered to result from recruitment, mortality, and re- 25.4°C, respectively). Onoue et al. (2006) revealed that gional distribution of the population within the bay. The adult copepods of A. steueri in Sagami Bay increased in seasonal abundance of this species differed greatly be- numbers with water temperature from February to June tween 2007 and 2009, i.e. absent in August and September and produced diapausing eggs from February to August. 2007 whereas it was abundant in the corresponding Since most diapausing eggs were produced in the early months of 2008. This may be due to differences in the re- summer with the maximum rate in June, they considered gional distribution of their populations in the bay between that A. steueri produced diapausing eggs to survive the the two years. high temperature season. In contrast, the A. steueri C2–C6 The seasonal succession of Acartia copepods in Okkirai population in Okkirai Bay completely disappeared from Bay can be summarized as follows. The dominant Acartia April to May or June, when the water temperature was species were A. longiremis in the colder season and A. below 11°C. Our preliminary laboratory rearing of A. steueri in the warmer season, followed by A. omorii or A. steueri collected from Okkirai Bay indicated that they pro- hudsonica. Acartia longiremis and A. omorii increased in duced diapausing eggs at the low temperatures prevalent in numbers sharply during the colder months (February to December (below 13°C). These results suggest that low April), probably by lateral advection of immigrants due to temperatures are not favorable for this copepod for growth intrusion of the Oyashio water, and then decreased with in- and reproduction and that they spend low-temperature pe- creasing water temperature. Acartia steueri occurred al- riods as diapausing eggs. most throughout the year except for the coldest season Compared to Acartia longiremis and A. steueri, the peak (March to May) when the copepod is considered to spend a abundances of A. omorii and A. hudsonica were low in Ok- phase as a diapausing egg. Acartia hudsonica exhibited a kirai Bay. According to Ueda (1987), A. omorii and A. hud- similar seasonal occurrence to A. omorii, but it was more sonica in Maizuru Bay, western Japan, exhibited almost abundant during the warmer months. Water temperature synchronous seasonal changes, but were more or less seg- and intrusion of the Oyashio Current water are thus major regated in their regional distributions; A. omorii was lo- environmental factors determining the seasonal succes- cated relatively more seaward than A. hudsonica. The sea- sions of Acartia species in Okkirai Bay. sonal occurrences of these species in Okkirai Bay were also similar to each other, but differed in the timing of Acknowledgments their peak abundances, i.e. in the colder months (April 2008 and February 2009) for A. omorii and the warmer We are grateful to Dr. Hiroshi Ueda and Dr. Susumu months (September 2008 and June 2009) for A. hudsonica Ohtsuka for their invaluable advice in identifying Acartia (Fig 4c,d). A possible reason for this difference is species- species. Part of this study was supported by JSPS KAK- specific seasonal variation in their regional distributions, ENHI Grant Number 21780183, and a Kitasato University which may result in different seasonal variations at a single Research Grant for Young Researchers. sampling station. The temporal differences in their peak abundances may be explained by the differences in their modes of recruit- References ment. 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